Pesticides, mortality and population growth rate

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22 McPhail, J.D. (1994) Speciation and the evolution of reproductive isolation in the sticklebacks (Gasterosteus): origin of sympatric pairs. In The Evolutionary Biology of the Threespine Stickleback (Bell, M.A. and Foster, S.A., eds), pp. 399– 347, Oxford University Press 23 Foster, S.A. et al. (1997) Patterns of homoplasy in behavioral evolution. In Homoplasy and the Evolutionary Process (Sanderson, M.J. and Hufford, L., eds), pp. 245 – 269, Academic Press 24 McKinnon, J.S. and Rundle, H.D. (2002) Speciation in nature: the threespine stickleback model systems. Trends Ecol. Evol. 17, 480 – 488 25 Amores, A.A. et al. (1998) Zebrafish hox clusters and vertebrate genome evolution. Science 282, 1711 – 1714 26 Tanaka, M. et al. (2002) Fin development in a cartilaginous fish and the origin of vertebrate limbs. Nature 416, 527 – 531 27 Kingsley, D.M. et al. New genomic tools for molecular studies of evolutionary change in stickleback. Behaviour (in press) 28 Ahn, D. and Gibson, G. (1999) Axial variation in the threespine stickleback: relationship to Hox gene expression. Dev. Genes Evol. 209, 473– 481 29 Cresko, W.A. et al. (2003) Genome duplication, subfunction partitioning, and lineage divergence: Sox9 in stickleback and zebrafish. Dev. Dyn. 228, 480– 489 30 Hosemann, K.E. et al. (2004) A simple and efficient microinjection protocol for making transgenic sticklebacks. Behaviour (in press)

0169-5347/$ - see front matter q 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2004.07.004

| Letters

Pesticides, mortality and population growth rate Benedikt R. Schmidt1,2 1 2

Zoologisches Institut, Universita¨t Zu¨rich, Winterthurerstrasse 190, 8057 Zu¨rich, Switzerland KARCH, Naturhistorisches Museum, Bernastrasse 15, 3005 Bern, Switzerland

In a recent article in TREE, Sih and colleagues point out that standard ecotoxicology tests might not be useful for assessing the real threat from a pesticide for non-target organisms [1]. Pesticide effects might be seriously underestimated if their interactive effects with other stressors, such as predators, are ignored [2,3]. This insight is important and will help to improve ecotoxicology tests. Yet, ecotoxicology testing, regardless of whether interactive effects are included, still has a major shortcoming. Typical ecotoxicology tests examine the effects of pesticides on single vital rates, usually mortality. Such individual-level responses are relatively easy to study and can provide important first insight. However, they do not inform us about whether the population as a whole will suffer [4]; from a conservation perspective, it is these population-level effects that matter [4]. Thus, ecotoxicology tests should be done at the population level, unless it can be shown that individual-level responses are good proxies for population-level responses. Responses of individuals might inform about population performance when mortality is very high. Often, however, mortality is intermediate and there can be sub-lethal effects [5]. As pointed out by Forbes and Calow, three questions need to Corresponding author: Benedikt R. Schmidt ([email protected]). Available online 15 July 2004 www.sciencedirect.com

be answered before the population-level effects of toxicants can be assessed [4]: (i) to what extent do individual-level variables underestimate or overestimate population-level responses?; (ii) how do toxicant-caused changes in individual-level variables translate into changes in population dynamics?; and (iii) to what extent are the population-level effects influenced by density-dependent (compensatory) responses? Studying the population-level effects of toxicants is a challenging task, but the experimental study by Forbes and colleagues shows that it can be done [6]. The link between individual-level and population-level responses is poorly understood in amphibians with complex life cycles [7,8]. Sih and colleagues discuss experiments carried out with larval amphibians, for which mortality was the response variable [2,3]. Population models suggest that the increased mortality in the tadpole stage has relatively minor effects on population growth [7,8], because density dependence is often strong in the tadpole stage [7]. Generally, terrestrial stages appear to be more important for the maintenance of positive population growth [7,8]. Although large-scale negative effects of pesticide use on amphibian populations have been shown in correlational studies [9], the work described by Sih and colleagues might help us to understand only a little about the processes leading to local and global

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amphibian population declines [10]. More research, preferably experimental and at the population level, is badly needed. Acknowledgements I thank Josh Van Buskirk for helpful comments and the Forschungskredit of the University of Zu¨rich for support.

References 1 Sih, A. et al. (2004) Two stressors are far deadlier than one. Trends Ecol. Evol. 19, 274 – 276 2 Relyea, R.A. (2002) Predator cues and pesticides: a double dose of danger for amphibians. Ecol. Appl. 13, 1515– 1521 3 Boone, M.D. and Semlitsch, R.D. (2001) Interactions of an insecticide with larval density and predation in experimental amphibian communities. Conserv. Biol. 15, 228 – 238 4 Forbes, V.E. and Calow, P. (2002) Population growth rate as a basis for ecological risk assessment of toxic chemicals. Philos. Trans. R. Soc. Lond. Ser. B 357, 1299– 1306

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5 Boone, M.D. and C.M. Bridges (2003) Effects of pesticides on amphibian populations. In Amphibian Conservation (Semlitsch, R.D., ed.), pp. 152– 167, Smithsonian Institution Press 6 Forbes, V.E. et al. (2003) Joint effects of population density and toxicant exposure on population dynamics of Capitella sp. I. Ecol. Appl. 13, 1094 – 1103 7 Vonesh, J.R. and De la Cruz, O. (2002) Complex life cycles and density dependence: assessing the contribution of egg mortality to amphibian declines. Oecologia 133, 325 – 333 8 Biek, R. et al. (2002) What is missing in amphibian decline research: insights from ecological sensitivity analysis. Conserv. Biol. 16, 728 – 734 9 Davidson, C. et al. (2002) Spatial tests of the pesticide drift, habitat destruction, UV-B, and climate-change hypotheses for California amphibian declines. Conserv. Biol. 16, 1588 – 1601 10 Houlahan, J.E. et al. (2000) Quantitative evidence for global amphibian population declines. Nature 404, 752 – 755 0169-5347/$ - see front matter q 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2004.06.006

| Letters Response

Response to Schmidt. Pesticides, mortality and population growth rate Andrew Sih1, Jake Kerby1, Alison Bell2 and Rick Relyea3 1

Department of Environmental Science and Policy, University of California, Davis, CA 95616, USA Environmental and Evolutionary Biology, University of Glasgow, UK, G12 8QQ 3 Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA 15260, USA 2

In his comment on our recent TREE report [1] about new work showing very strong synergistic effects of pesticides and predation risk on tadpole mortality [2], Schmidt makes two important points [3]: (i) individual effects (e.g. behavior or mortality) do not necessarily translate into population effects; and (ii) if there is strong density dependence in the larval stage, enhanced tadpole mortality might not be very important. We agree with his basic points, but come to a different conclusion. Schmidt concludes that the work described in our report ‘might help us to understand only a little about the processes leading to local and global amphibian population declines’ [3]. By contrast, we suggest that studies on individual responses are a crucial part of an integrative approach to understanding multiple stressor impacts on natural populations. Our view is based on both conceptual and practical grounds. From a conceptual perspective, we believe that an ideal approach should blend individual and population-level studies to gain a multi-level integrative mechanistic understanding of factors governing population performance [4]. Whereas Schmidt [3], following Forbes and Calow [5], emphasizes that it is difficult to predict population performance from individual effects, we emphasize the flipside – that it is difficult to understand population and community dynamics without studying individual Corresponding author: Andrew Sih ([email protected]). Available online 24 June 2004 www.sciencedirect.com

responses [6]. In particular, understanding how individuals cope (or do not cope) with conflicting demands is likely to be crucial for understanding multiple stressor impacts on populations. From a practical perspective, although it is easy to suggest that we should study impacts of toxicants (and, ideally, synergistic effects of toxicants and natural biotic stressors) on populations, this is a ‘challenging task’, as Schmidt [3] notes. In his article [3], Schmidt also emphasizes that work by Forbes and colleagues [7] shows that it can be done; however, this study was carried out on a small, relatively immobile, short-lived (with a generation time of a few weeks) invertebrate. Comparable studies on amphibians would take years, probably decades, and should be done on a metapopulation landscape scale. Doing this for one species is challenging; doing it for hundreds of amphibian species and tens of thousands of registered chemicals is infeasible. A practical alternative is to make inroads by studying individual-level responses to multiple stressors in multiple life-history stages. Schmidt’s other main point (drawn from [8]), that strong density dependence can make the larval stage relatively unimportant to population ecology, is intriguing. The implication is that exposure to pesticides and predation risk (predator cues), which caused up to 90% larval mortality in just a few days, might be unimportant. This criticism potentially applies not only to ecotoxicology, but also to larval amphibian ecology in general. Have